Catalase/peroxidases (KatGs) are bifunctional haem b-containing (Class I) peroxidases with overwhelming catalase activity and substantial peroxidase activity with various one-electron donors. These unique oxidoreductases evolved in ancestral bacteria revealing a complex gene-duplicated structure. Besides being found in numerous bacteria of all phyla, katG genes were also detected in genomes of lower eukaryotes, most prominently of sac and club fungi. Phylogenetic analysis demonstrates the occurrence of two distinct groups of fungal KatGs that differ in localization, structural and functional properties. Analysis of lateral gene transfer of bacterial katGs into fungal genomes reveals that the most probable progenitor was a katG from a bacteroidetes predecessor. The putative physiological role(s) of both fungal KatG groups is discussed with respect to known structure–function relationships in bacterial KatGs and is related with the acquisition of (phyto)pathogenicity in fungi.

Introduction

H2O2 is a harmful metabolic by-product of aerobic life that also acts as second messenger in signal transduction pathways [1]. During cellular evolution, its rapid and effective removal by various oxidoreductases was of essential importance. Cells evolved not only enzymes capable of efficient dismutation of H2O2 [i.e. haem catalases, manganese catalases and KatGs (catalase/peroxidases)], but also enzymes that reduce hydrogen peroxide with the help of various organic and inorganic one- and two-electron donors (haem peroxidases and non-haem peroxidases, e.g. peroxiredoxins).

KatGs represent one of the most abundant families of Class I of the non-animal haem peroxidase superfamily [2]. They are unique in accomplishing efficiently both catalatic and peroxidatic activity with various substrates [3]. Most currently known KatG representatives (360 sequences at present) are encoded in bacterial genomes, and mechanistic knowledge about these peculiar bifunctional peroxidases has derived from studies on bacterial and archaeal species [4]. In contrast, eukaryotic KatGs, abundant mainly among fungi and protists, have hardly been described.

It is a well-known phenomenon that LGT (lateral gene transfer) has often occurred in the evolutionary history between all three domains of cellular life, i.e. Archaea, Bacteria and Eukarya [5]. We have reconstructed the LGT from ancient bacteria into fungal genomes and discuss the functional implications in the present paper. Phylogenetic and sequence analysis reveals the presence of two distinct groups of fungal representatives, namely of intracellular and extracellular KatGs. On the basis of both multiple sequence alignment and known structure–function relationships of bacterial enzymes, these two groups are critically analysed with respect to (putative) enzymatic and functional properties.

Data mining

For multiple sequence alignment and phylogenetic analysis, complete protein sequences of 49 haem KatGs were used, including all 36 currently known fungal KatG sequences (updated from all databases in March 2009; see Table 1). For comparison, 13 selected bacterial KatGs known already from previous work [2] were added. All used protein sequences and their corresponding ID-numbers and genes can be followed in PeroxiBase [6].

Table 1
Alphabetical list of 49 protein sequences used for phylogenetic analyses

Members of Group 1 of (intracellular) fungal peroxidases are designated KatG1, whereas extracellular KatGs are designated KatG2. Sequences deposited in databases as ‘KatG3 (*)’ are actually KatG1 paralogues, as shown in the text. Alternative names for some sequences are also shown.

Abbreviation PeroxiBase ID Organism Phylum 
AclKatG1 3409 Aspergillus clavatus Ascomycota 
AflKatG1 3394 Aspergillus flavus Ascomycota 
AfumKatG1 1881 Aspergillus fumigatus Ascomycota 
AniKatG1 (AniCpeA) 1905 Aspergillus nidulans Ascomycota 
AnKatG1 (AnCpeB) 5224 Aspergillus niger Ascomycota 
AorKatG1 3448 Aspergillus oryzae Ascomycota 
AteKatG1 3413 Aspergillus tereus Ascomycota 
BBFLKatG1 3590 Flavobacteria bacterium BBFL7 Bacteroidetes 
BBFLKatG2 3610 Flavobacteria bacterium BBFL7 Bacteroidetes 
BfKatG 2290 Burkholderia xenovorans (formerly Burkholderia fungorumProteobacteria 
BgKatG1 (BgCPX) 1960 Blumeria graminis Ascomycota 
BpKatG 2303 Burkholderia pseudomallei Proteobacteria 
CgKatG1 3408 Chaetomium globosum Ascomycota 
EcoHPI 2394 Escherichia coli Proteobacteria 
EcoKatP 2386 Escherichia coli Proteobacteria 
FjKatG 3617 Flavobacterium johnsoniae Bacteroidetes 
FoKatG1 5228 Fusarium oxysporum Ascomycota 
FoKatG2 5229 Fusarium oxysporum Ascomycota 
FoKatG3* 5353 Fusarium oxysporum Ascomycota 
FtKatG 2678 Francisella tularensis Proteobacteria 
GmoKatG1 3415 Gibberella moniliformis Ascomycota 
GmoKatG2 3414 Gibberella moniliformis Ascomycota 
GzKatG1 2477 Gibberella zeae Ascomycota 
GzKatG2 2338 Gibberella zeae Ascomycota 
GzKatG3* 5354 Gibberella zeae Ascomycota 
HjKatG1 2539 Hypocrea jecorina (Trichoderma reeseiAscomycota 
HjKatG2 5459 Hypocrea jecorina (Trichoderma reeseiAscomycota 
HmaKatG1 2440 Haloarcula marismortui Euryarchaeota 
MagKatG1 2288 Magnaporthe grisea Ascomycota 
MagKatG2 2337 Magnaporthe grisea Ascomycota 
MgKatG1 2538 Mycosphaerella graminicola Ascomycota 
MtuKatG 3571 Mycobacterium tuberculosis Actinobacteria 
NcKatG1 (NcCat2) 2181 Neurospora crassa Ascomycota 
NfKatG1 3412 Neosartorya fischeri Ascomycota 
NhaeKatG1 5480 Nectria haematococca Ascomycota 
NhaeKatG2 5374 Nectria haematococca Ascomycota 
PanKatG1 5373 Podospora anserina Ascomycota 
PenchrKatG1 6601 Penicillium chrysogenum Ascomycota 
PEspKatG 5801 Pedobacter sp. Bacteroidetes 
PmKatG1 (PmCPE1) 2182 Penicilium marneffei Ascomycota 
PnoKatG1 3449 Phaeosphaeria nodorum Ascomycota 
PtritKatG1 5798 Pyrenophora tritici-repentis Ascomycota 
SspKatG1 2714 Synechococcus sp. Cyanobacteria 
SyspKatG1 2479 Synechocystis sp. Cyanobacteria 
TatKatG1 5797 Trichoderma atroviride Ascomycota 
TatKatG2 5800 Trichoderma atroviride Ascomycota 
TstKatG1 5796 Talaromyces stipitatus Ascomycota 
TviKatG1 5799 Trichoderma virens Ascomycota 
UmKatG1 2327 Ustilago maydis Basidiomycota 
Abbreviation PeroxiBase ID Organism Phylum 
AclKatG1 3409 Aspergillus clavatus Ascomycota 
AflKatG1 3394 Aspergillus flavus Ascomycota 
AfumKatG1 1881 Aspergillus fumigatus Ascomycota 
AniKatG1 (AniCpeA) 1905 Aspergillus nidulans Ascomycota 
AnKatG1 (AnCpeB) 5224 Aspergillus niger Ascomycota 
AorKatG1 3448 Aspergillus oryzae Ascomycota 
AteKatG1 3413 Aspergillus tereus Ascomycota 
BBFLKatG1 3590 Flavobacteria bacterium BBFL7 Bacteroidetes 
BBFLKatG2 3610 Flavobacteria bacterium BBFL7 Bacteroidetes 
BfKatG 2290 Burkholderia xenovorans (formerly Burkholderia fungorumProteobacteria 
BgKatG1 (BgCPX) 1960 Blumeria graminis Ascomycota 
BpKatG 2303 Burkholderia pseudomallei Proteobacteria 
CgKatG1 3408 Chaetomium globosum Ascomycota 
EcoHPI 2394 Escherichia coli Proteobacteria 
EcoKatP 2386 Escherichia coli Proteobacteria 
FjKatG 3617 Flavobacterium johnsoniae Bacteroidetes 
FoKatG1 5228 Fusarium oxysporum Ascomycota 
FoKatG2 5229 Fusarium oxysporum Ascomycota 
FoKatG3* 5353 Fusarium oxysporum Ascomycota 
FtKatG 2678 Francisella tularensis Proteobacteria 
GmoKatG1 3415 Gibberella moniliformis Ascomycota 
GmoKatG2 3414 Gibberella moniliformis Ascomycota 
GzKatG1 2477 Gibberella zeae Ascomycota 
GzKatG2 2338 Gibberella zeae Ascomycota 
GzKatG3* 5354 Gibberella zeae Ascomycota 
HjKatG1 2539 Hypocrea jecorina (Trichoderma reeseiAscomycota 
HjKatG2 5459 Hypocrea jecorina (Trichoderma reeseiAscomycota 
HmaKatG1 2440 Haloarcula marismortui Euryarchaeota 
MagKatG1 2288 Magnaporthe grisea Ascomycota 
MagKatG2 2337 Magnaporthe grisea Ascomycota 
MgKatG1 2538 Mycosphaerella graminicola Ascomycota 
MtuKatG 3571 Mycobacterium tuberculosis Actinobacteria 
NcKatG1 (NcCat2) 2181 Neurospora crassa Ascomycota 
NfKatG1 3412 Neosartorya fischeri Ascomycota 
NhaeKatG1 5480 Nectria haematococca Ascomycota 
NhaeKatG2 5374 Nectria haematococca Ascomycota 
PanKatG1 5373 Podospora anserina Ascomycota 
PenchrKatG1 6601 Penicillium chrysogenum Ascomycota 
PEspKatG 5801 Pedobacter sp. Bacteroidetes 
PmKatG1 (PmCPE1) 2182 Penicilium marneffei Ascomycota 
PnoKatG1 3449 Phaeosphaeria nodorum Ascomycota 
PtritKatG1 5798 Pyrenophora tritici-repentis Ascomycota 
SspKatG1 2714 Synechococcus sp. Cyanobacteria 
SyspKatG1 2479 Synechocystis sp. Cyanobacteria 
TatKatG1 5797 Trichoderma atroviride Ascomycota 
TatKatG2 5800 Trichoderma atroviride Ascomycota 
TstKatG1 5796 Talaromyces stipitatus Ascomycota 
TviKatG1 5799 Trichoderma virens Ascomycota 
UmKatG1 2327 Ustilago maydis Basidiomycota 

Multiple sequence alignment

Multiple sequence alignment was performed with Clustal X, version 2.0 [7]. The following optimized parameters were used: for pairwise alignments, gap opening penalty 9, gap extension penalty 0.1, and for multiple alignment, gap opening penalty 8, gap extension penalty 0.2. Residue-specific penalties and hydrophilic penalties were activated, and the gap separation distance was set to 4. Gonnet protein weight matrix was used and the delay-divergent cut off was optimized to 23%.

Phylogenetic analysis

Phylogenetic reconstruction with the distance method was performed with the Mega package, version 4.1 [8]. The following optimized parameters were used: JTT matrix, pairwise deletion of gaps, gamma distribution of mutation rates with gamma optimized to 1.85. As a test of inferred phylogeny, 1000 bootstrap replicates were used. The reconstructed majority rule consensus tree was presented with the Tree Explorer of the same Mega package.

Phylogenetic reconstruction using the MP (maximum parsimony) method was accomplished also within the Mega package [8]. Parameters were optimized as follows: CNI (close-neighbour-interchange) with search level 2 was selected with the initial tree formed by random addition with 200 replicates, and all alignment sites were used for this method.

Phylogenetic reconstruction with the ML (maximum-likelihood) method was performed within the PHYLIP package, version 3.68 [9]. The ProML program with JTT matrix and gamma distribution was applied (gamma was optimized to 1.85). For statistical purposes, 100 bootstrap replicates were applied, and the consensus tree was formed with the Tree Consense program of the same PHYLIP package.

Signal sequence prediction

Putative signal sequences were detected using the predictive algorithm of the program SignalP at http://www.cbs.dtu.dk/services/SignalP. The available eukaryotic signal sequence database was chosen for this prediction [10].

Evolutionary relationships

The molecular evolutionary relationships within a group of 36 fungal and 13 bacterial katG genes (Table 1) have been analysed by application of three distinct phylogenetic methods, namely (i) NJ (neighbour-joining) distance method, (ii) MP method, and (iii) ML method. The resulting reconstructed unrooted tree obtained by using the whole coding regions is presented in Figure 1. Very similar tree topologies were obtained with the three approaches. The condensed NJ-tree is displayed with statistical support from 1000 bootstrap replications. Figure 1 clearly demonstrates that fungal katG genes have segregated in two distinct groups.

Reconstructed unrooted phylogenetic tree of 36 fungal KatGs and 13 selected bacterial counterparts

Figure 1
Reconstructed unrooted phylogenetic tree of 36 fungal KatGs and 13 selected bacterial counterparts

The condensed NJ tree is shown, but very similar topologies were obtained using the MP method and the ML method. Bootstrap values in the nodes were obtained from NJ/MP/ML methods respectively. Alternative names and PDB codes of known structures are given in parentheses.

Figure 1
Reconstructed unrooted phylogenetic tree of 36 fungal KatGs and 13 selected bacterial counterparts

The condensed NJ tree is shown, but very similar topologies were obtained using the MP method and the ML method. Bootstrap values in the nodes were obtained from NJ/MP/ML methods respectively. Alternative names and PDB codes of known structures are given in parentheses.

Group 1 comprises more representatives (denominated KatG1) and includes both pathogenic and non-pathogenic fungi. The only currently known basidiomycete representative, a plant pathogen (i.e. Ustilago maydis), falls in this group. The reconstructed phylogenetic tree suggests that Group 1 can be divided into three major clades. The first clade contains genes from phytopathogenic and saprobic ascomycetes. Recently, the successful heterologous expression and preliminary biochemical characterization of Magnaporthe grisea KatG1, a representative of clade 1, has been reported [11]. The second clade is also represented by mainly phytopathogenic fungi and includes several Gibberella and Fusarium species that even have two KatG1-encoding genes. These katG1 sequences are paralogues, i.e. they derive from a recent intraspecies gene duplication event. Finally, aspergilli sequences of both pathogenic and non-pathogenic species dominate the third clade of Group 1. This clade includes the gene encoding Penicillium marneffei KatG that has been demonstrated to be induced in the virulent yeast phase of this dangerous human pathogen [12].

Group 2 (denominated KatG2) can be divided into two subclades. The two Trichoderma sequences were segregated rather early, whereas all six remaining KatG2 representatives are phytopathogenic sac fungi. It is interesting to see that all members of Group 2 have a N-terminal sequence for protein secretion (Table 2), whereas all members of Group 1 are intracellular proteins with high structural and functional similarities to their bacterial counterparts [11]. It is important to note that signal sequences for secretion are found also in a few bacterial KatGs but not in bacteroidetes (Table 2), which are phylogenetically closely related to fungal KatGs (Figure 1) and might be at the origin of the eukaryotic enzymes (see below). This suggests that the ascomycete-specific signal sequence has been acquired later on by adaptive evolution of KatGs from Group 2. This adaptation step resulted in unique extracellular KatGs that could be effectively involved in fungal defence against oxidative burst during plant attack [13]. This is underlined by the fact that expression of KatG2, but not KatG1, is enhanced under oxidative stress conditions [11]. In any case, only pathogenic fungi encode both KatG1 and KatG2.

It was proposed previously [2] that eukaryotic katG genes arose via LGT from bacterial genomes. Sequence analysis of the katG1 promoter region as well as of the adjacent non-coding DNA region preceding the M. grisea katG1 gene gave further evidence for LGT of only the KatG-coding region [11]. Phylogenetic reconstruction described in the present paper has revealed details of LGT from bacteria towards ancient fungi. This work demonstrates that two katG genes (both yet putative) from flavobacteria and sphingobacteria are the closest phylogenetic neighbours of all fungal KatGs (Figure 1, bacteroidetes clade). The data presented might indicate that LGT of katG genes has contributed to acquisition of pathogenicity in fungi during their adaptive evolution, consistent with previous investigations that demonstrated the role of horizontal (lateral) gene transfer in the evolution of pathogenicity in various bacteria [14]. It has to be noted that bacteroidetes are strictly anaerobic bacteria nevertheless possessing enzymes for effective degradation of reactive oxygen species.

Table 2
Alphabetical list of protein sequences revealing signal sequences for secretion [10]

All members of Group 2 (KatG2) have an N-terminal signal sequence, whereas members of Group 1 (KatG1) do not have a signal sequence.

Abbreviation Organism Signal sequence length (amino acids); first native amino acid Signal peptide probability (hidden Markov model) 
AflKatG1 Aspergillus flavus Non-secretory 0.000 
BBFLKatG1 Flavobacteria bacterium BBFL7 Non-secretory 0.267 
BBFLKatG2 Flavobacteria bacterium BBFL7 Non-secretory 0.000 
EcoKatP Escherichia coli 23; alanine 1.000 
FjKatG Flavobacterium johnsoniae Non-secretory 0.000 
FoKatG1 Fusarium oxysporum 18; glutamine 0.998 
FoKatG2 Fusarium oxysporum 18; glutamine 0.999 
FoKatG3 Fusarium oxysporum Non-secretory 0.224 
GmoKatG1 Gibberella moniliformis Non-secretory 0.231 
GmoKatG2 Gibberella moniliformis 18; glutamine 0.999 
GzKatG2 Gibberella zeae 18; aspartic acid 1.000 
HjKatG2 Hypocrea jecorina (Trichoderma reesei18; isoleucine 0.997 
MagKatG2 Magnaporthe grisea 23; glutamine 1.000 
NhaeKatG2 Nectria haematococca 21; aspartic acid 1.000 
PEspKatG Pedobacter sp. Non-secretory 0.000 
TatKatG2 Trichoderma atroviride 18; valine 0.999 
Abbreviation Organism Signal sequence length (amino acids); first native amino acid Signal peptide probability (hidden Markov model) 
AflKatG1 Aspergillus flavus Non-secretory 0.000 
BBFLKatG1 Flavobacteria bacterium BBFL7 Non-secretory 0.267 
BBFLKatG2 Flavobacteria bacterium BBFL7 Non-secretory 0.000 
EcoKatP Escherichia coli 23; alanine 1.000 
FjKatG Flavobacterium johnsoniae Non-secretory 0.000 
FoKatG1 Fusarium oxysporum 18; glutamine 0.998 
FoKatG2 Fusarium oxysporum 18; glutamine 0.999 
FoKatG3 Fusarium oxysporum Non-secretory 0.224 
GmoKatG1 Gibberella moniliformis Non-secretory 0.231 
GmoKatG2 Gibberella moniliformis 18; glutamine 0.999 
GzKatG2 Gibberella zeae 18; aspartic acid 1.000 
HjKatG2 Hypocrea jecorina (Trichoderma reesei18; isoleucine 0.997 
MagKatG2 Magnaporthe grisea 23; glutamine 1.000 
NhaeKatG2 Nectria haematococca 21; aspartic acid 1.000 
PEspKatG Pedobacter sp. Non-secretory 0.000 
TatKatG2 Trichoderma atroviride 18; valine 0.999 

Essential residues and motifs

Multiple sequence alignment reveals a high level of conservation along the whole coding region (see Supplementary Figure S1 at http://www.biochemsoctrans.org/bst/037/bst0370772add.htm). On the distal side of the prosthetic haem group (Supplementary Figure S1A), the catalytic triad found in all Class I peroxidases (that include in addition ascorbate and cytochrome c peroxidases) is strictly conserved: Arg87–Trp90-His91 (M. grisea KatG1 numbering) [3]. Moreover, all complete sequences quoted in Table 1 show the presence of Asn121 (hydrogen-bonding partner of distal His91), Asp120 (controls access of H2O2 to the active site) and the peculiar KatG-typical covalent adduct Trp90–Tyr238–Met264 that is essential for the catalase, but not the peroxidase, activity of this unique oxidoreductase [15,16]. Regarding the proximal haem side (Supplementary Figure S1B), the triad His279–Trp330–Asp389 is also fully conserved in both groups of fungal KatGs [3]. These findings suggest that the principal mechanism of bifunctional activity as well as enzymatic parameters might be similar in prokaryotic and eukaryotic enzymes. So far, this has been demonstrated only for M. grisea KatG1 [11], but needs to be demonstrated for representatives of Group 2.

katG genes are the result of an ancestral gene duplication event [17] comprising an N-terminal haem-containing domain and a C-terminal domain without prosthetic group. Supplementary Figures S1C and S1D present highly conserved motifs from the C-terminal domain that resemble the distal and proximal side of the (N-terminal) haem cavity. Essential distal and proximal histidine residues are replaced by Ala486 and Leu630 respectively, thereby preventing haem binding, although other typical distal and proximal sequence motifs are highly conserved in the duplicated domain both in archaeal/bacterial and eukaryotic KatGs. The functional consequences of this two-domain structure are not fully understood. The C-terminal domain has been described to be essential for restructuring the active centre in the N-terminal domain [18], thereby promoting the correct architecture for the bifunctional activity of KatG [19]. This has been shown for bacterial KatGs [18,19], and it is reasonable to assume that identical structure–function relationships are valid in the (two-domain) eukaryotic enzymes.

In both fungal KatG groups, a putative gene fusion of katG with another coding region was detected (Aspergillus flavus KatG1 and Gibberella zeae KatG2; see Supplementary Table S1 at http://www.biochemsoctrans.org/bst/037/bst0370772add.htm). In the case of intracellular KatG from Aspergillus flavus (known to produce aflatoxin), katG1 is fused with a gene encoding a (putative) protein of the major facilitator protein family known to mediate transport of substances across membranes [20]. In the case of extracellular G. zeae KatG2, the situation is even more complicated. According to gene prediction, extracellular (soluble) KatG2 might be anchored by a transmembrane anchor that is fused with an intracellular cytochrome P450 domain with homology with family 7-A (see Supplementary Figure S2 at http://www.biochemsoctrans.org/bst/037/bst0370772add.htm). Clearly, it has to be investigated whether these multidomain proteins are expressed completely and are (multi)functional enzymes in vivo. The inducible expression of sole KatG2 has already been described [21], and the spliced mRNA sequence obtained has been submitted to the EST (expressed sequence tag) database (accession number FD528596). Heterologous expression and characterization of recombinant G. zeae KatG2 is currently underway (P.G. Furtmüller, C. Obinger and M. Zámocký, unpublished work).

Protein Evolution: Sequences, Structures and Systems: Biochemical Society Focused Meeting to commemorate the 200th Anniversary of Charles Darwin's birth held at the Wellcome Trust Conference Centre, Cambridge, U.K., 26–27 January 2009. Organized and Edited by Roman Laskowski (EMBL-EBI, Hinxton, U.K.), Michael Sternberg (Imperial College London, U.K.) and Janet Thornton (EMBL-EBI, Hinxton, U.K.).

Abbreviations

     
  • KatG

    catalase/peroxidase

  •  
  • LGT

    lateral gene transfer

  •  
  • ML

    maximum likelihood

  •  
  • MP

    maximum parsimony

  •  
  • NJ

    neighbour-joining

Funding

This work was supported by the Austrian Science Fund FWF Project No. P20996.

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